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During their first mission, they encountered activity on the Romulan Neutral Zone when a group of Romulan starships began attacking an unidentified Vulcan ship. Whilst investigating the incident, a planet was destroyed through unknown means, crippling the Stargazer and leaving Captain Ruhalter critically wounded. The next high ranking officer, Jean-Luc Picard, took command of the ship during the encounter. Ruhalter died of his injuries, and when the ship returned to Starbase 61, Picard was given command, a position he would hold for the next 22 years. (STvideo game: Legacy)

A different account of Picard's ascension to the captaincy is told in The Valiant.

In 2339, the Stargazer came under attack by an 11-million-year-old automated defense system. Just before the star became a red giant, the native civilization had attempted to stop its expansion. Instead, the attempt caused solar eruptions, and the entire civilization was forced to abandon the system. Captain Picard ordered the Stargazer into a gap in the weapons' coverage, allowing science officerValderrama to deactivate it.

The Stargazer accidentally jumped forward in time ten days in 2341 by a tiny quantum singularity that was responsible for the orbital irregularity of a binary system. When the Stargazer attempted to warp away from the singularity, it instead leapt forward in time, causing the warp nacelles to stay in temporal sync with their previous timeframe. First officerJack Crusher deduced that emitting a series of graviton pulses from ten light-days away would resynchronize the engines with the rest of the ship, allowing the Stargazer to continue (TNGnovel: The Buried Age). Around this time, the Stargazer returned to Earth for an extensive overhaul and refitting (TNGepisode: "We'll Always Have Paris").

In 2345, the ship took fire while surveying an ice giant. After a warning shot, the Stargazer was contacted briefly by aquatic beings that lived in the water-ammonia mantle of the planet. Dubbed "Polyphemians" by Captain Picard, they requested no further contact, as previous interactions with Class-M-life forms had been harmful to both parties.

Captain Picard ordered his helm to obtain a bearing on the attacking vessel, and upon receiving that bearing ordered his ship to jump into high warp for several seconds. He then ordered the ship to come to a full stop near the unknown ship. As a result, the Stargazer briefly appeared to be in two places at once - and the Seventy-Fifth Rule fired where the Stargazer had been. The Stargazer fired phasers and six photon torpedoes at the ship, which exploded.

Afterwards, Captain Picard decided to abandon the Stargazer, which was on fire and losing power. The survivors of the battle drifted in shuttlecraft for weeks before being picked up. Upon his return to the Federation, Captain Picard was court martialed for the loss of the Stargazer, but was ultimately acquitted. The desperate maneuver Picard used at the battle would come to be known as the Picard Maneuver.

Shortly after the battle, a starship commanded by Bok entered the system in search of the Seventy-Fifth Rule, but only the stricken Stargazer was found in decaying orbit of Maxia Zeta V. Against many of his crews wishes and risking trouble from his superiors, DaiMonBok took control of the Stargazer as a personal prize in the hopes of one day hatching a plot for revenge against Picard. Over the years, Bok used scavenged parts and components purchased from corrupt Federation dealers to restore the Stargazer to the point where, apart from some slight structural damage, she was fully operational once more. (TNGepisode: "The Battle"; novel: The Buried Age)

In 2364, Bok asked for a meeting with the USS Enterprise-D. At the initial meeting Bok formally returned the Stargazer to Federation control. It was at this point that Starfleet finally learned the identity of the unknown vessel that attacked the Stargazer, that it had been a Ferengi starship.

What Bok had not revealed at the initial meeting was that his son had been in command, that he was on his first voyage as a DaiMon when Picard destroyed his ship. Bok was using the Stargazer as part of an elaborate scheme to take revenge on Picard. He had planted a mind altering device in Picard's quarters on the Stargazer, Picard unknowingly took the device back to the Enterprise. This device permitted Bok to control Picard's mind to the point where Picard was reliving his experiences on the Stargazer just prior to the battle.

Bok used the device to get Picard on board the Stargazer, in the hopes that in his confused state Picard would mistake the Enterprise for the attacking Ferengi ship and destroy them. Picard, convinced he was at the Battle of Maxia, tried to attack the Enterprise using the Picard Maneuver - however Data had constructed a defense to the Picard Maneuver and kept Picard from attacking his own ship.

Bok was arrested and removed from power by his first officer. Following the incident, a tug met the Enterprise, and towed the Stargazer to a nearby starbase. (TNGepisode: "The Battle")